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Echography of the Cervix and Uterus During the Proliferative and Secretory Phases of the Menstrual Cycle in Bonnet Monkeys (Macaca Radiata)

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Echography of the Cervix and Uterus During the Proliferative and Secretory Phases of the Menstrual Cycle in Bonnet Monkeys (Macaca Radiata) Journal of the American Association for Laboratory Animal Science Vol 53, No 1 Copyright 2014 January 2014 by the American Association for Laboratory Animal Science Pages 18–23 Echography of the Cervix and Uterus during the Proliferative and Secretory Phases of the Menstrual Cycle in Bonnet Monkeys (Macaca radiata) Uddhav K Chaudhari,1,* Siddnath M Metkari,2 Dhyananjay D Manjaramkar,2 Geetanjali Sachdeva,1 Rajendra Katkam,1 Atmaram H Bandivdekar,3 Abhishek Mahajan,4 Meenakshi H Thakur,4 and Sanjiv D Kholkute1 We undertook the present study to investigate the echographic characteristics of the uterus and cervix of female bonnet monkeys (Macaca radiata) during the proliferative and secretory phases of the menstrual cycle. The cervix was tortuous in shape and measured 2.74 ± 0.30 cm (mean ± SD) in width by 3.10 ± 0.32 cm in length. The cervical lumen contained 2 or 3 col- liculi, which projected from the cervical canal. The echogenicity of cervix varied during proliferative and secretory phases. The uterus was pyriform in shape (2.46 ± 0.28 cm × 1.45 ± 0.19 cm) and consisted of serosa, myometrium, and endometrium. The endometrium generated a triple-line pattern; the outer and central lines were hyperechogenic, whereas the inner line was hypoechogenic. The endometrium was significantly thicker during the secretory phase (0.69 ± 0.12 cm) than during the proliferative phase (0.43 ± 0.15 cm). Knowledge of the echogenic changes in the female reproductive organs of bonnet monkeys during a regular menstrual cycle may facilitate understanding of other physiologic and pathophysiologic changes. Ultrasound imaging is a noninvasive, atraumatic, and simple Materials and Methods method to assess various organs in humans and nonhuman pri- Animals and husbandry practices. Adult female bonnet macaques 11 mates. Ultrasonography has been used to detect fetal growth, (Macaca radiate; n = 15) showing normal menstrual cycles under- endometrial thickness, and endometriosis in rhesus macaques went abdominal ultrasonography during their late proliferative 17,20,26 (Macaca mulatta), and color Doppler ultrasonography (days 6 through 13) and midsecretory (days 16 through 21) phases. has used for characterizing uteroplacental hemodynamics and Bonnet monkeys used in the present study were wild-caught from 22,29 assessing fetal and placental blood flow in that species. In a forest in southern India. Monkeys were housed individually and cynomolgus macaques (Macaca fascicularis), ultrasound tech- fed with fresh seasonal vegetables, fruits, ground nuts, bangal niques have been applied in transfundal uterine sperm recovery, grams, and so forth. Water was provided ad libitum. Housing follicular fluid aspiration, assessment of endometrial changes conditions were a 12:12-h light:dark cycle, with a temperature of during the menstrual cycle, evaluation of folliculogenesis, 24 to 28 °C and relative humidity of 30% to 70%. Previous reports 5,33-35 and ovulation induction studies. Other primates species from our laboratory have shown that the length of menstrual wherein ultrasound techniques have been used are vervet mon- cycle in bonnet monkeys is 25 to 30 d.6,24 Menstrual cyclicity was 31 30 keys (Cercopithecus aethiops), owl monkeys (Aotus nancymaae), monitored for at least 2 cycles by daily vaginal swab examination 9,12 and common marmosets (Callithrix jacchus). at 1100. The day of visible vaginal bleeding was considered as Bonnet macaques (Macaca radiata) have been used as an animal day 1, and ultrasonography was performed on days 6 through 6,23,24 model for research on contraceptive agents, endometrial 13 (proliferative phase) and 16 through 21 (secretory phases). The 18,27,28 10 biology, and assisted reproductive technologies. Al- ultrasound protocol was approved by the Institutional Animal though bonnet macaques bear close similarity with rhesus Ethics Committee, and ultrasound examinations were performed macaques, ultrasound profile of cervix and uterus in these spe- during routine health monitoring of bonnet monkeys in the colony. cies has not yet been characterized. We undertook the present To ensure that the monkey’s urinary bladders should be full dur- study to evaluate the echographic profile of the cervix and ing ultrasound examination, water bowls were removed during uterus in regularly cycling bonnet macaques in the proliferative the evening prior to the exam and replaced the morning of the (days 6 through 13 after overt bleeding) and secretory phases ultrasonography. The animal facility at the institute is registered (days 16 through 21) of menstrual cycle. Knowledge of the nor- with the Committee for the Purpose of Control and Supervision of mal ultrasonographic profiles of the female reproductive organs Experiments on Animals, Ministry of Social Justice and Empower- may facilitate the identification of pathophysiological changes ment, Government of India (registration no. 78/1999/CPCSEA). during natural or stimulated cycles in bonnet monkeys. Gynecologic ultrasound examination. A gynecologic ultrasound evaluation of the cervix and uterus was performed in B mode by Received: 22 May 2013. Revision requested: 03 Jul 2013. Accepted: 11 Jul 2013. using high-resolution linear curved transducers (L12-5 MHz and 1Department of Primate Biology, 2Animal House Facility, and 3Department of Biochem- C5-2 MHz probes, HDXE11 ultrasound system, Philips, Andover, istry, National Institute for Research in Reproductive Health (NIRRH), Indian Council MA). The shape, echogenic texture, position, and dimensions of of Medical Research (ICMR), Parel, Mumbai, India; 4Department of Radiodiagnosis, Tata Memorial Hospital (TMH), Parel, Mumbai, India. the cervix and uterus were studied during the late proliferative *Corresponding author. Email: [email protected] and midsecretory phases of the menstrual cycle. Monkeys were 18 Ultrasonography of reproductive organs Figure 1. An ultrasound image of the reproductive organs of bonnet monkeys obtained by using the C5-2 probe during (A) late proliferative and (B) midsecretory phases of the menstrual cycle, demonstrating the echogenicity of the uterus and cervix during the proliferative (hypoechoic) and midsecretory (hyperechoic) phases. The cervical canal appears open and filled with mucus during the proliferative phase compared with secretory phase. C, cervix; CC, cervical canal; CrDC, cranial dorsal colliculus; CuDC, caudal dorsal colliculus; Is, isthmus; U, uterus; UC, uterine cavity; V, vagina; VC, ventral colliculus. Figure 2. An ultrasound image of the cervix of bonnet monkeys during the late proliferative phase of the menstrual cycle, obtained by using the L12-3 probe. (A) Sagittal view. (B) Transverse view. The cervical canal appears open and contains mucus, and colliculi are separated and distinctly visible. CC, cervical canal; CrDC, cranial dorsal colliculus; CW, cervical wall; VC, ventral colliculus. sedated with ketamine (10 mg/kg body weight) and placed in a RWave Cardio Products, Mumbai, India) was applied to the shaved supine position. The region was disinfected (Savlon, Johnson and area. Initially the entire reproductive tract was examined by using Johnson, Mumbai, India), and the hair was shaved from 2/3 of the the C5-2MHz transducer. The transducer was placed sagittally abdominal cavity, to the pubic symphysis. Ultrasound gel (RTrace, on the lower midline of the pelvic–abdominal region to locate the 19 Vol 53, No 1 Journal of the American Association for Laboratory Animal Science January 2014 Figure 3. An ultrasound image of the cervix of bonnet monkeys during the midsecretory phase of the menstrual cycle, obtained by using the L12-3 probe. (A) Sagittal view. (B) Transverse view. The cervical canal appears collapsed, and colliculi are merged. CC, cervical canal; CrDC, cranial dorsal colliculus; CuDC, caudal dorsal colliculus; VC, ventral colliculus. vagina, cervix, and uterus. The linear L12-5 MHz transducer then Table 1. Cervical, uterine, and endometrial measurements (cm; mean was used for individual examination of the cervix and uterus. The ± SD) during the late proliferative and midsecretory phases of the uterus was localized in the lower 2/3 of the abdominal area. The menstrual cycle of bonnet monkeys cervix was localized above the pubic symphysis. The craniocaudal Late proliferative Midsecretory and dorsoventral diameters of the cervix, uterus, and endometrium Cervix were measured from sagittal scans, and the transverse diameters of Craniocaudal diameter 2.74 ± 0.30 2.69 ± 0.24 these organs were obtained from transverse scans.16 Four observa- Dorsoventral diameter a b tions were made for each monkey during both the proliferative and 3.10 ± 0.32 2.88 ± 0.37 secretory phases of the menstrual cycle. The cervix was measured Transverse diameter 2.86 ± 0.28 2.62 ± 0.27 from the internal os to external os (craniocaudal diameter) and from Uterus the dorsal colliculi to ventral colliculi (dorsoventral diameter). The Craniocaudal diameter 2.46 ± 0.28 2.41 ± 0.32 uterus was measured from the outer body of uterus (fundus) to the Dorsoventral diameter 1.45 ± 0.19a 1.39 ± 0.24b internal os of the cervix to obtain the craniocaudal and dorsoventral Transverse diameter 1.42 ± 0.37 1.52 ± 0.42 diameters (extending from the dorsal to the ventral side of uterus). Endometrium The endometrium appeared as a triple-line pattern consisting of Craniocaudal diameter 1.20 ± 0.23 1.34 ± 0.42 a prominent outer and central hyperechogenic lines and an inner Dorsoventral diameter 0.43 0.15c 0.69 0.12c hypoechogenic or black region on
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